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Title: Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus

Abstract

White-rot (WR) fungi are pivotal decomposers of dead organic matter in forest ecosystems and typically use a large array of hydrolytic and oxidative enzymes to deconstruct lignocellulose. However, the extent of lignin and cellulose degradation may vary between species and wood type. Here, we combined comparative genomics, transcriptomics and secretome proteomics to identify conserved enzymatic signatures at the onset of wood-decaying activity within the Basidiomycota genus Pycnoporus. We observed a strong conservation in the genome structures and the repertoires of protein-coding genes across the four Pycnoporus species described to date, despite the species having distinct geographic distributions. We further analysed the early response of P. cinnabarinus, P. coccineus and P. sanguineus to diverse (ligno)-cellulosic substrates. We identified a conserved set of enzymes mobilized by the three species for breaking down cellulose, hemicellulose and pectin. The co-occurrence in the exo-proteomes of H2O2-producing enzymes with H2O2-consuming enzymes was a common feature of the three species, although each enzymatic partner displayed independent transcriptional regulation. Finally, cellobiose dehydrogenase-coding genes were systematically co-regulated with at least one AA9 lytic polysaccharide monooxygenase gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood-decaying process.

Authors:
 [1];  [2];  [2];  [3];  [2];  [3];  [3];  [3];  [2];  [2];  [4];  [4];  [4];  [5];  [5];  [5];  [6];  [5];  [7];  [7] more »;  [8];  [9];  [10];  [11];  [11];  [12];  [13];  [10];  [5];  [12]; ORCiD logo [14];  [15];  [15];  [5];  [16];  [17];  [14];  [5];  [4];  [18]; ORCiD logo [4] « less
+ Show Author Affiliations
  1. Aix Marseille Univ. (France). Biodiversity and Biotechnology of Fungi. INRAE; Université de Lorraine, Nancy (France). Interactions Arbres/Microorganismes. INRAE
  2. Aix Marseille Univ. (France). Biodiversity and Biotechnology of Fungi. INRAE
  3. Aix Marseille Univ. (France). Biodiversity and Biotechnology of Fungi. INRAE; Aix Marseille Univ. (France). INRAE. CIRM-CF
  4. INRAE, UMR1163, Biodiversity and Biotechnology of Fungi, Aix Marseille University, 13009 Marseille, France
  5. US Department of Energy, Joint Genome Institute, Walnut Creek, CA, USA
  6. INRAE, UMR1319, Micalis, Plateforme d’Analyse Protéomique de Paris Sud-Ouest, Jouy-en-Josas, France
  7. INRAE, Genotoul Bioinfo, UR875, Mathématiques et Informatique Appliquées de Toulouse, Castanet-Tolosan, France
  8. USDA Forest Products Laboratory, Madison, WI, USA
  9. Fungal Physiology, Westerdijk Fungal Biodiversity Institute and Fungal Molecular Physiology, Utrecht University, Utrecht, The Netherlands; Department of Microbiology, University of Helsinki, Helsinki, Finland
  10. Department of Biology, Southeast Missouri State University, Cape Girardeau, MI, USA
  11. CNRS, UMR7257, AFMB, Aix Marseille University, Marseille, France; INRAE, USC1408, AFMB, Marseille, France
  12. Department of Microbiology, University of Helsinki, Helsinki, Finland
  13. Department of Molecular Wood Biotechnology and Technical Mycology, Büsgen-Institute, Georg-August-University Göttingen, Göttingen, Germany; Center for Molecular Biosciences (GZMB), Georg-August-University Göttingen, Göttingen, Germany
  14. Centro de Investigaciones Biológicas, CSIC, Madrid, Spain
  15. INRAE, UMR1136, Interactions Arbres/Microorganismes, Université de Lorraine, Nancy, France
  16. Molecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, The Netherlands
  17. Microbiology, Utrecht University, Utrecht, The Netherlands
  18. US Department of Energy, Joint Genome Institute, Walnut Creek, CA, USA; Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
Contributing Org.:
UMR INRAE Research Collaboration
OSTI Identifier:
1816251
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
DNA Research
Additional Journal Information:
Journal Volume: 27; Journal Issue: 2; Journal ID: ISSN 1340-2838
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Miyauchi, Shingo, Hage, Hayat, Drula, Elodie, Lesage-Meessen, Laurence, Berrin, Jean-Guy, Navarro, David, Favel, Anne, Chaduli, Delphine, Grisel, Sacha, Haon, Mireille, Piumi, François, Levasseur, Anthony, Lomascolo, Anne, Ahrendt, Steven, Barry, Kerrie, LaButti, Kurt M., Chevret, Didier, Daum, Chris, Mariette, Jérôme, Klopp, Christophe, Cullen, Daniel, de Vries, Ronald P., Gathman, Allen C., Hainaut, Matthieu, Henrissat, Bernard, Hildén, Kristiina S., Kües, Ursula, Lilly, Walt, Lipzen, Anna, Mäkelä, Miia R., Martinez, Angel T., Morel-Rouhier, Mélanie, Morin, Emmanuelle, Pangilinan, Jasmyn, Ram, Arthur F. J., Wösten, Han A. B., Ruiz-Dueñas, Francisco J., Riley, Robert, Record, Eric, Grigoriev, Igor V., and Rosso, Marie-Noëlle. Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus. United States: N. p., 2020. Web. doi:10.1093/dnares/dsaa011.
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Miyauchi, Shingo, Hage, Hayat, Drula, Elodie, Lesage-Meessen, Laurence, Berrin, Jean-Guy, Navarro, David, Favel, Anne, Chaduli, Delphine, Grisel, Sacha, Haon, Mireille, Piumi, François, Levasseur, Anthony, Lomascolo, Anne, Ahrendt, Steven, Barry, Kerrie, LaButti, Kurt M., Chevret, Didier, Daum, Chris, Mariette, Jérôme, Klopp, Christophe, Cullen, Daniel, de Vries, Ronald P., Gathman, Allen C., Hainaut, Matthieu, Henrissat, Bernard, Hildén, Kristiina S., Kües, Ursula, Lilly, Walt, Lipzen, Anna, Mäkelä, Miia R., Martinez, Angel T., Morel-Rouhier, Mélanie, Morin, Emmanuelle, Pangilinan, Jasmyn, Ram, Arthur F. J., Wösten, Han A. B., Ruiz-Dueñas, Francisco J., Riley, Robert, Record, Eric, Grigoriev, Igor V., & Rosso, Marie-Noëlle. Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus. United States. https://doi.org/10.1093/dnares/dsaa011
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Miyauchi, Shingo, Hage, Hayat, Drula, Elodie, Lesage-Meessen, Laurence, Berrin, Jean-Guy, Navarro, David, Favel, Anne, Chaduli, Delphine, Grisel, Sacha, Haon, Mireille, Piumi, François, Levasseur, Anthony, Lomascolo, Anne, Ahrendt, Steven, Barry, Kerrie, LaButti, Kurt M., Chevret, Didier, Daum, Chris, Mariette, Jérôme, Klopp, Christophe, Cullen, Daniel, de Vries, Ronald P., Gathman, Allen C., Hainaut, Matthieu, Henrissat, Bernard, Hildén, Kristiina S., Kües, Ursula, Lilly, Walt, Lipzen, Anna, Mäkelä, Miia R., Martinez, Angel T., Morel-Rouhier, Mélanie, Morin, Emmanuelle, Pangilinan, Jasmyn, Ram, Arthur F. J., Wösten, Han A. B., Ruiz-Dueñas, Francisco J., Riley, Robert, Record, Eric, Grigoriev, Igor V., and Rosso, Marie-Noëlle. Wed . "Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus". United States. https://doi.org/10.1093/dnares/dsaa011. https://www.osti.gov/servlets/purl/1816251.
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@article{osti_1816251,
title = {Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus},
author = {Miyauchi, Shingo and Hage, Hayat and Drula, Elodie and Lesage-Meessen, Laurence and Berrin, Jean-Guy and Navarro, David and Favel, Anne and Chaduli, Delphine and Grisel, Sacha and Haon, Mireille and Piumi, François and Levasseur, Anthony and Lomascolo, Anne and Ahrendt, Steven and Barry, Kerrie and LaButti, Kurt M. and Chevret, Didier and Daum, Chris and Mariette, Jérôme and Klopp, Christophe and Cullen, Daniel and de Vries, Ronald P. and Gathman, Allen C. and Hainaut, Matthieu and Henrissat, Bernard and Hildén, Kristiina S. and Kües, Ursula and Lilly, Walt and Lipzen, Anna and Mäkelä, Miia R. and Martinez, Angel T. and Morel-Rouhier, Mélanie and Morin, Emmanuelle and Pangilinan, Jasmyn and Ram, Arthur F. J. and Wösten, Han A. B. and Ruiz-Dueñas, Francisco J. and Riley, Robert and Record, Eric and Grigoriev, Igor V. and Rosso, Marie-Noëlle},
abstractNote = {White-rot (WR) fungi are pivotal decomposers of dead organic matter in forest ecosystems and typically use a large array of hydrolytic and oxidative enzymes to deconstruct lignocellulose. However, the extent of lignin and cellulose degradation may vary between species and wood type. Here, we combined comparative genomics, transcriptomics and secretome proteomics to identify conserved enzymatic signatures at the onset of wood-decaying activity within the Basidiomycota genus Pycnoporus. We observed a strong conservation in the genome structures and the repertoires of protein-coding genes across the four Pycnoporus species described to date, despite the species having distinct geographic distributions. We further analysed the early response of P. cinnabarinus, P. coccineus and P. sanguineus to diverse (ligno)-cellulosic substrates. We identified a conserved set of enzymes mobilized by the three species for breaking down cellulose, hemicellulose and pectin. The co-occurrence in the exo-proteomes of H2O2-producing enzymes with H2O2-consuming enzymes was a common feature of the three species, although each enzymatic partner displayed independent transcriptional regulation. Finally, cellobiose dehydrogenase-coding genes were systematically co-regulated with at least one AA9 lytic polysaccharide monooxygenase gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood-decaying process.},
doi = {10.1093/dnares/dsaa011},
journal = {DNA Research},
number = 2,
volume = 27,
place = {United States},
year = {Wed Apr 01 00:00:00 EDT 2020},
month = {Wed Apr 01 00:00:00 EDT 2020}
}
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